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First published online September 5, 2008
Journal of Experimental Biology 211, 3009-3019 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018895
Consequences of buoyancy to the maneuvering capabilities of a foot-propelled aquatic predator, the great cormorant (Phalcrocorax carbo sinensis)
1 Department of Biology, Technion, Haifa 32000, Israel
2 Faculty of Aerospace engineering, Technion, Haifa 32000, Israel
* Author for correspondence at present address: Department of Biology, University of South Dakota, Vermillion, SD 57069, USA (e-mail: gal.ribak{at}gmail.com)
Accepted 20 June 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: maneuverability, locomotion, swimming, diving, torque, pitch, trim-control
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Webb, 2002;
Weihs, 1993;
Weihs, 2002). The term
maneuver describes unsteady aspects of motion and can also be used to describe
changes in swimming speed without a change in swimming direction (i.e.
accelerating and braking). However, here, we refer exclusively to the ability
and limits of making a controlled change to the swimming direction. Turning
involves accelerating normal to the instantaneous direction of swimming. Since
this centripetal acceleration is a function of tangential speed and trajectory
radius these two parameters have been widely used to characterize the
maneuvering performance of various swimmers (e.g.
Blake et al., 1995;
Fish, 2002;
Fish and Nicastro, 2003;
Fish et al., 2003a;
Rivera et al., 2006;
Walker, 2000). However, these
two parameters per se cannot explain how animals control their
maneuvers or highlight the factors limiting maneuverability. To obtain such
insights, one must explore how the organism maneuvers (e.g.
Fish and Nicastro, 2003;
Webb and Weihs, 1983). In the
present study, we report on the hydrodynamic mechanism used by cormorants to
maneuver in the vertical plane.
Cormorants are foot-propelled aquatic predators that rely exclusively on
submerged swimming for capturing fish
(Johnsgard, 1993). They are
extremely efficient aquatic predators, reportedly yielding some of the highest
catch per unit effort recorded for avian divers
(Grémillet et al.,
2001). They achieve this remarkable foraging performance despite a
limited adaptation for a pelagic life style. Like several other avian divers,
cormorants utilize the aquatic media while retaining full flight capabilities.
The primary adaptation of the avian body for flight results in low specific
density. Underwater this translates into avian divers being among the most
buoyant pelagic swimmers (Lovvorn and Jones, 2004;
Wilson et al., 1992). The high
buoyancy is due to the light skeletons of birds and the large air volumes
carried underwater inside the body (air sacs) and trapped in the plumage.
Enstipp et al. showed that the energy expenditure of swimming cormorants
changes with dive depth (Enstipp et al.,
2006). Water depth provides relief from buoyancy to deep divers by
compressing the air volumes in the body. However, great cormorants seldom dive
to depths exceeding 10 m (Grémillet
et al., 1999). As a result, they forage in the part of the water
column where their swimming is affected by their positive buoyancy.
Understanding how cormorants cope with their buoyancy to maneuver efficiently
underwater is an important step for a better understanding of the foraging
behavior and habitat selection (e.g. preferred foraging depth) in these
aquatic predators.
Cormorants use foot-propulsion for swimming underwater. During swimming,
the wings are folded next to the body and do not participate in swimming
(Johnsgard, 1993). As a
result, the body of cormorants is deprived of median control surfaces that are
used for trim-control in many fish and marine mammals
(Fish, 2002;
Fish and Shannahan, 2000;
Webb and Weihs, 1983). While
swimming horizontally in a straight line, cormorants do so with their body
inclined (pitch) at a negative angle-of-attack (AoA) to the swimming
direction. This produces hydrodynamic lift forces that are directed downward
and help the bird overcome its buoyancy while swimming horizontally
(Ribak et al., 2004;
Ribak et al., 2006). The
angles of the body and tail alternate during the paddling cycle, suggesting
that the birds are using their flat tails as hydrofoils to regulate the pitch
angle of the body. By tilting it independently from the body, the tail can
generate lift from the motion of the bird through the water, and the resulting
moment can be used to pitch the body and control its cyclic rotation through
the paddling cycle. The angle of the body, in turn, can regulate the lift
forces produced by the body and the tail. When their buoyancy was artificially
reduced by attaching weights to the body, cormorants swimming in a straight
horizontal trajectory reduced their body angle to reduce the vertical forces
produced during swimming (Ribak et al.,
2006). This suggests that the birds can regulate the dynamic
forces produced during swimming to achieve equilibrium of forces with changing
buoyancy in the vertical axis. Since the dynamic forces are a result of the
swimming speed of the birds, the birds may require a minimum swimming speed to
maintain such an equilibrium. However, cormorants need to do more than swim in
a straight horizontal line, and by controlling the magnitude of vertical
forces the birds may be able to control their trajectory. How they actually do
this is demonstrated in the present study.
We report on an experiment designed to explore the mechanism for pitch control and vertical maneuvering in shallow-swimming great cormorants. Since the birds actively resist buoyancy during swimming we hypothesized that maneuvers in the vertical plane will involve shifting the equilibrium of the normal forces produced during swimming with buoyancy to result in a net normal force in the desired direction. Since the normal forces produced during swimming are hydrodynamic and derived from the swimming speed of the birds, we expected the birds to maintain a minimal swimming speed throughout the maneuver for generating sufficient lift by the body and tail. The inability of the birds to slow down would result in a limit to the maneuvering capabilities (turning radius). To test these ideas experimentally, we constructed a submerged obstacle course that forced the birds to perform a vertical maneuver by swimming in a bell-shaped trajectory. We tested the maneuvering limitation of the birds by progressively increasing the difficulty of the obstacle course. The swimming of the birds through the obstacle course was filmed and analyzed to reveal how the birds control their trajectory and orientation.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Ribak et al.,
2005; Ribak et al.,
2006) and were housed in the same aviary and pool described
therein. Hence, only a brief description of the facilities is provided
below. The birds were trained to enter a pool (8x5 m, 1 m deep) one at a time and dive from one end of the pool to the other through a 7 m-long, submerged enclosure (`channel') with a rectangular cross section (0.5x0.5 m) made of metal fencing (mesh size, 0.02x0.05 m). The channel was placed on the bottom of the pool. Starting 3.5 m away from the entrance to the channel, a 2 m-long section of the channel was used as the test section. It was filmed from the side using submerged video camera that covered the section and a 45 deg. inclined mirror placed above the section. The mirror provided an upper view of the channel. The birds were motivated to dive through the channel by rewarding them with fish at one end. At the time of the experiment, the birds were familiar with the channel and the pool and were routinely diving from one side of the channel to the other as part of their weekly training protocol conducted for over one year. For the experiment reported in the present study, we altered the channel described above by adding thin, 0.25 m-high vertical barriers made of the same metal mesh as the channel. The barriers were put in place to block the passage through the upper or lower half of the tunnel (Fig. 1). At the center of the test section one barrier (B0.5) was placed to block the passage through the lower half of the tunnel. Two additional barriers were placed at equal distances along the channel length on either side of B0.5 (B0 towards the entrance and B1 towards the exit). B0 and B1 blocked the passage through the upper half of the channel. Two additional barriers were placed further towards the entrance to the channel, also blocking the upper half of the channel, to ensure that the birds reached B0 after swimming in the lower half of the channel.
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We filmed the birds swimming through the obstacle course (one at a time) at
six difficulty levels when the horizontal distance between the barriers was
90, 70, 55, 45, 40 and 36 cm. Each bird was filmed swimming through the
channel several times. We discarded sequences in which the birds were seen to
touch any of the barriers. In the remaining sequences we measured the duration
(number of video fields, 50 fields s–1) of when the tip of
the bill passed beneath B0 to the time when the tip of the tail
passed beneath B1. The shortest sequence for each bird in each
maneuvering level was used for further analysis as it represented the maximum
performance for that bird at that maneuvering level. In these sequences, for
each video field, we digitized the positions
(Fig. 2): of the tip of the
tail (P1); the base of the tail (P2); a marker (a 1.5 cm-diameter circle
divided by its radii into six equal areas with alternate colors of red and
yellow printed on a 2x2 cm yellow adhesive tape), which was glued
(SuperWiz, Loctite; Rocky Hill, Connecticut, USA) to the wing feathers,
approximating the position of the center of mass
(Ribak et al., 2004) along the
major axis of the body (P3); the point between the neck and body (P4); the tip
of the bill (P5); the base of the foot (P6); and the tip of the longest digit
(P7). Additionally, five points between P4 and P5 were digitized in sequence
(N1–N5) from the neck to the bill. They did not correspond to specific
landmarks on the neck but were all placed on the mid-line of the neck and head
as observed in the images. All the points described above were digitized in
the side view of the birds. In the upper view (through the mirror), we only
digitized the tip of the bill (P5), the point of connection between the neck
and body (P4) and the tip of the tail (P1) for calibration purposes (distance
from the camera) and to ensure that no significant lateral perturbation of the
body, neck or tail was evident in the movies.
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Motion analysis from video
All analysis was performed in 2-D, focusing only on the vertical plane
where the trajectory of the birds occurred. The horizontal axis (x)
was chosen parallel to the length of the channel, with positive values
increasing in the horizontal direction of swimming. The vertical axis
(y) was positive in the direction pointing upward. The walls of the
tunnel prevented the birds from having a lateral component of motion, thus
justifying the 2-D approach. We used the marker point on the body to calculate
the swimming speed and trajectory of the birds from the videos. Swimming speed
was calculated from the change in position of the center of mass (P3) along
the horizontal and vertical axes between fields (time) using numerical
derivation [four points parabola approximation
(Rayner and Aldridge, 1985)].
A second time derivative provided the acceleration. The components of velocity
were used to trigonometrically calculate the instantaneous swimming direction,
and the velocity and acceleration components were used to calculate the
instantaneous turning radius (R) from the curvature
(kxy) of the trajectory of the birds in the vertical
plane:
 | (1) |
T) and body (B),
respectively. B was numerically derived with respect to time
(as described above for swimming speed) to obtain the angular velocity and
angular acceleration of the body. As for the data for the turning radius, we
calculated the mean angular velocity of the body for each maneuvering
difficulty level only when the values were negative corresponding to the
nose-down rotation at the center of the obstacle course. The coordinates of
points P4 and P5 provided a robust description of the pitch angle of the neck
(N). A more accurate description accounting for the
flexibility of the neck is provided below also using points N1–N5 (see
estimation of forces). To compare the swimming of the birds at the different levels of maneuvers we used a non-dimensional axis where the x-axis for each difficulty level was adjusted so that the position of B0.5 was assigned a value of 0.5 (arbitrary units) and B0 and B1 were 0 and 1.0, respectively. As a result, the adjusted axes represent the horizontal position inside the obstacle course relative to the barriers rather than the actual position.
The fields in which the birds were observed paddling were noted during the analysis. We considered birds to be paddling in fields where the foot was seen to move backwards and up relative to the body. Throughout this work variation among the eight birds is reported as ± s.d.
Estimation of forces
We previously estimated the vertical forces produced by the body, tail and
feet of cormorants during straight horizontal swimming using a quasi-steady
approach and technical data taken from published wind tunnel studies on
geometrical shapes (Ribak et al.,
2004). Whenever possible we followed the same estimation method
here. However, several adjustments were required for the more complex case of
swimming in a curved path. We therefore describe in detail the points
differing from our previous analysis
(Ribak et al., 2004) and only
mention briefly the methods adopted from our original study.
Usually, during straight, horizontal swimming the neck is stretched forward
and the head points in the swimming direction
(Ribak et al., 2004). However,
this was not the case when the birds maneuvered. We therefore modeled the
contribution of the neck and head to the forces and moments used for turning.
To account for the bending of the long, flexible neck during maneuvers we used
the digitized data from points P4, P5 and N1–5. For each time step
(video field), we used these seven points as nodes to interpolate (using
cubic-spline.) 24 equally spaced points representing 23 cross sections along
the neck and head. This allowed us to treat the neck flexibility by modeling
it as a sum of 23 finite elements, each oriented differently with respect to
the flow. The most anterior section corresponds to the pointed tip of the bill
and consequently was not included in the estimation. For each of the remaining
22 elements we calculated the instantaneous velocity from the distance moved
between fields as described above. Each section was assumed to be a fixed
length cylinder (l=1.5 cm) aligned with the length of the neck. The angle of
the length of each section relative to the direction of velocity of the
section is the angle-of-attack of the section (). Each section was
assigned a different diameter (d) based on actual diameters measured
from a cormorant neck in fig. 1 in Ribak et al.
(Ribak et al., 2005). To model
the hydrodynamic forces produced by each section we used the cross-flow
principle (Hoerner, 1965). A
cylinder with its length inclined with respect to the flow at an angle
produces a hydrodynamic force normal to the length of the cylinder
(FN). This force can be estimated as:
 | (2) |
 | (3) |
is water density (1000 kg m–3) and u is
speed. CD is the drag coefficient of the cylinder (based
on frontal area) when the cylinder is oriented normal to the direction of
flow. We used CD=1.1 as in fig. 18, p. 3–11 in
(Hoerner, 1965).
The normal forces from all 22 neck sections were combined using vector
summation to give the total force generated by the neck. Because we were
interested in how the birds control their maneuvers we also summed the moments
generated by each neck section. The moment generated by the i-th neck section
was estimated as the cross product of the 2-D vector connecting P3 to the i-th
neck section (ri) and FNi. The moment
(M) generated by the neck was calculated by summing the moments of the
different sections:
 | (4) |
For the hydrodynamic forces generated by the tail, we previously used an
approximation to a delta-shaped hydrofoil experiencing flow deflected by the
body (Ribak et al., 2004). In
a subsequent study (Ribak et al.,
2006), we noted that this is a good approximation only when the
body and tail are at small AoA (<15 deg.), as in the case of rapid swimming
in a straight line. When the birds were swimming more slowly, they tilted
their body further, exposing parts of the tail directly to the free stream
flow (Ribak et al., 2005;
Ribak et al., 2006).
Consequently, in the present study where the birds were forced to slow down
and were tested on their ability to rotate their body within the maneuver, we
considered the tail as a delta-shaped hydrofoil experiencing flow from its
motion relative to the water, independent of the wake of the body. We took the
center of the dynamic pressure of the tail to be located at 0.6 of the
distance between the base of the tail and tip of the tail, as suggested by the
delta wing model (Hoerner and Borst,
1985). The instantaneous position of this hydrodynamic center was
used to calculate the velocity of this point in the videos as described above.
The geometric AoA of the tail was calculated from T and the
direction of velocity of the tail. We calculated the CL
and CD coefficients for the tail from the
leading-edge-suction analogy (Polhamus,
1971). This calculation requires only the measured AoA of the tail
and coefficients for the potential flow (kp=1.3) and vortex lift
(kv=3.15) that are obtained from charts [fig. 3 in Polhamus
(Polhamus, 1968)] based on
aspect-ratio of the tail [AR=1.0
(Ribak et al., 2004)].
The CL and CD coefficients of a
thin delta wing with sharp edges are then calculated as:
 | (5) |
 | (6) |
 | (7) |
 | (8) |
)]. We were
then able to calculate the resultant force vector for the tail, which acts at
the center of pressure of the tail. From the force vector and the distance
between the center of pressure and P3, we calculated the turning moment that
the tail exerts on the body, similar to Eqn
4.
For the lift forces produced by the tilted body we used the same estimation
method described previously (Ribak et al.,
2004). Lift is calculated using
Eqn 7, where the
CL is taken from the AoA of the body () and wind
tunnel data on streamlined bodies (CL=0.008).
CL is based on a characteristic area (A=0.0225
m2), which is the square of the maximum width (left to right) of
the body. As we were primarily interested in forces with a component normal to
the swimming direction that can be used for maneuvering, we did not need to
calculate the drag of the body, which, by definition, is in the direction of
swimming. Drag and lift generated by the body can contribute to pitching the
body when the hydrodynamic center of the body is anterior or posterior to the
center of mass. As there are no data to indicate otherwise, we assume here
that in cormorants the hydrodynamic center is close enough to the center of
mass, thus resulting in zero pitch.
Finally, since the birds paddled at all of the maneuver levels, we also
added the contribution of thrust generated by the feet during the stroke phase
using the same estimation approach described previously
(Ribak et al., 2004). The
thrust of the feet is assumed to be the vector sum of lift, drag and inertia
(acceleration reaction, including the virtual mass of the feet). The
estimation of force assumes that the feet function as a low aspect-ratio
(AR=4), thin hydrofoil moving at an arch beneath the body at speed,
acceleration and AoA derived from the kinematics of points P6 and P7 in the
video. This estimation, based on a 2-D view, ignores lateral forces that
should cancel out due to the symmetry of synchronized strokes where both feet
paddle together at the same time. We also disregarded any forces that might be
introduced by the feet during the recovery phase of the paddling cycle when
the webbed toes are adducted.
To elucidate the mechanism of maneuvering and to test whether the forces
calculated are realistic we summed the contribution of the different body
parts to the forces normal to the instantaneous direction of swimming. We then
compared this sum with the centrifugal force and the component of buoyancy
that a 2 kg bird (the mean body mass of the birds used) would encounter while
moving in the bell-shaped trajectory inside the obstacle course. Buoyancy
estimates (B=2.3 N kg–1) were based on empirical
measurements from carcasses reported previously (Ribak et al.,
2004). The component of
buoyancy that is normal to the swimming direction (Bsin β, where
β is the angle between the direction of buoyancy and the direction of
swimming velocity) was added to the centrifugal force
(Fcg), which acts normal to the direction of swimming. The
centrifugal force was calculated as:
 | (9) |
 | (10) |
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)], where
the birds were swimming through the same channel but with no vertical barriers
(no maneuvers). Table 1
summarizes some of the observed differences in maneuvering kinematics between
the different maneuver levels. At the tightest maneuver, the instantaneous
ac peaked when the bird was above B0.5,
reaching values of >1.5g (where g is
gravity). Fig. 5 shows the
change in pitch angle (relative to the horizon) of the body, neck and tail as
the birds passed through the obstacle course. Pitch angles oscillated while
the birds were passing through the obstacle course but there was a phase shift
between the three body parts (tail, body and neck). As a result, the neck and
tail were deflected relative to the angle of the body
(Fig. 6). The interesting point
to note in Fig. 6 is that the
birds are moving their tail and neck relative to their body in a similar
manner in all of the maneuvering difficulty levels but the amplitude of the
motions increases as the maneuver becomes tighter.
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In most cases, the birds were observed to paddle three times in each of the video sequences. The first stroke was typically before B0. The second stroke was performed between the two outer barriers in the vicinity of B0.5, and the third stroke was either before or after the birds passed beneath B1. However, there was high variability among the birds, and within the actions of individual birds, especially in the tighter turns. It seemed that the birds tended not to paddle near B0 (Fig. 7). In a few cases, the birds seemed to slow down the recovery phase between the first and second stroke, which might have helped them to slow down before reaching B0.5; however, this observation was not consistent in all the birds or trials.
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DISCUSSION |
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We chose to focus on vertical rather than horizontal maneuvers and on
bell-shaped maneuvers rather than simple turns for three reasons. First,
cormorants are foot-propelled divers powered by their webbed feet, which are
located posterior and ventral to the center of mass of the body. This results
in a cyclic body pitching during each paddling cycle where the stroke is
performed when the body is at maximum pitch
(Ribak et al., 2004).
Cormorants use the lift from their body to resist their buoyancy and direct
thrust vertically. This swimming strategy seems well adapted for buoyant
divers needing to swim horizontally underwater. However, foraging is not
limited to horizontal trajectories and the asymmetry of foot propulsion in
cormorants (in the dorsoventral axis) raises the question of how the birds
control their trajectory when large pitch angles are needed to maneuver in the
vertical plane? The bell-shaped, vertical trajectory reveals the birds'
ability to control their trajectory by forcing them to alternate swimming
direction between both sides of the body (ventral and dorsal) as well as to
regulate the magnitude of the forces and moments produced during swimming. We
elaborate further on this asymmetry below.
The second reason for focusing on vertical maneuvers has to do with
swimming stability. When thrust is produced posterior to the center of mass,
swimming is unstable because a slight perturbation causing the center of mass
to deviate from the line of action of thrust (e.g. a sudden pitch) will result
in a larger torque, further increasing the perturbation
(Weihs, 2002). By contrast,
when thrust is produced anterior to the center of mass the design is stable
and perturbations will subside passively. Wing-propelled birds have their
wings close to the center of mass, resulting in a more stable trim-control.
Many fish and marine mammals generate thrust posterior to the center of mass
but they also posses fins anterior to the center of mass that can stabilize
the pitch of the body (Fish,
2000; Webb and Weihs,
1983). Cormorants do not have such stabilizers, and the only
horizontal surface is the tail that is posterior to the body. The maneuver
described here enables the evaluation of the function of the tail as a pitch
control device by comparing the motions of the tail with the angular
acceleration of the body.
More importantly, the bell-shaped maneuver allows distinction between the pitch control function of the tail and the heave (normal acceleration) function. Fig. 9 shows that when the bird is between B0 and B0.5 the tail produces a normal force directed above the trajectory of the bird. This force is correlated with a negative moment generated by the tail and a change in direction of the angular acceleration of the body (clockwise) but not with the requirements for normal force equilibrium, which would suggest a negative force (Fig. 10). Thus, the bell-shaped maneuver provides evidence to support our hypothesis that the predominant function of the tail is probably pitch control.
The third reason is that understanding pitch control in cormorants is also fundamental for horizontal turning. Videos of cormorants performing 90 deg. horizontal turns show that the birds roll their body in order to perform banked turns, with the ventral side of the birds facing the center of the turn. Thus, for horizontal sideways turns, the birds are rolling to pitch the body as they turn. Although in the present study, we report only on the maneuvering of the birds in the vertical plane the insights are relevant for maneuvering in general.
For buoyant cormorants, any swimming direction other than vertical results in a component of buoyancy that is out of plane relative to the swimming direction. If the birds stop actively swimming, their trajectory will change due to the unbalanced action of buoyancy. Hence, because of buoyancy the swimming of cormorants is inherently unstable in the vertical plane. This has an implication for maneuvering that does not exist in neutrally buoyant swimmers. Vertical maneuvers in great cormorants are not symmetrical. Fig. 10 shows that the forces required to change swimming direction by a few degrees upwards are not the same as the forces required to make the same change downwards. The estimation of forces produced by the birds at different stages of the maneuver show that during the first third of the maneuver the birds changed their swimming direction almost passively by relaxing the forces resisting buoyancy and allowing buoyancy to divert them upwards. In the second third of the maneuver the birds were producing the highest normal forces to stop their acceleration upwards and convert the trajectory of the body downwards against buoyancy. It was at this stage that the birds tended to paddle the most.
Vertical maneuvers are asymmetric not just because of the direction of
buoyancy. The body of the birds is asymmetrical in the dorso–ventral
axis and the feet of cormorants are ventral to the body. We previously
estimated that the thrust produced by the feet of cormorants during shallow
horizontal swimming is equally directed forward and down
(Ribak et al., 2004). Thus,
much of the propulsive force can be used to produce a downwards curved
swimming direction but this is associated with a nose-up pitching moment
generated by the feet. Indeed, cormorants swimming in a constant direction
have a slightly undulating trajectory where the swimming direction is curved
downwards during the active phase of the paddling cycle and curves up during
the passive (recovery and glide) phase. At the same time, the oscillating
pitch of the body is adjusted so that the stroke starts when the body is at
maximum pitch. This undulation during horizontal swimming seems to be
regulated by the tail (Ribak et al.,
2004). While maneuvering, the asymmetry in propulsive force can
imply that the birds that were performing a tight maneuver with their ventral
side inside the turn may not be able to replicate such a tight maneuver if the
barriers were changed to invert the bell-shaped trajectory, forcing the birds
to make a tight turn with their dorsal side facing into the turn. Thus, tight
maneuvers in cormorants are probably active (i.e. the birds paddle throughout
the maneuver) not only to maintain swimming speed but also to contribute
normal forces for one-sided (ventral to the bird) vertical maneuvering. Figs
9 and
10 show that without foot
propulsion the normal forces produced by the body and tail would only be half
of the requirement for a downward-directed curved trajectory needed above
B0.5.
Our experiment shows that the birds reduced their swimming speed by only 12% between unobstructed swimming and the tightest maneuver possible. When evaluating this observation it should be noted that we used a gradual experimental design in which the difficulty level (trials) of the obstacle course increased in correlation with trial order. This was done to test the maximum maneuvering capabilities of the birds. In theory such a gradual design has the potential of incorporating gradual learning into the results. To eliminate this potential we allowed the birds to train at each difficulty level for two days prior to the measurement. This training ensured that the birds were already familiar with the course at the time of measurement.
The reason that the birds hardly reduced their swimming speed is likely to be a consequence of the mechanism employed by cormorants to maneuver. To change the direction of swimming the birds must produce a centripetal acceleration with a magnitude proportional to the square of swimming speed and inversely proportional to the turning radius (Eqn 10). As the birds perform a tighter maneuver, the turning radius will decrease and the required centripetal acceleration will increase unless the speed is reduced further. For great cormorants foraging at shallow depth, slowing down is not an option. Except for the thrust produced by the feet, all the normal hydrodynamic forces are derived from the swimming speed of the body. If the birds slow down, the normal turning force needed to change the swimming trajectory will decrease but so will the normal forces produced by the birds. The birds are probably reluctant to swim at lower speeds because the normal hydrodynamic forces produced would be too small to allow them precise control over their swimming direction. The combined action of the hydrodynamic forces with buoyancy to determine the dynamic equilibrium of the forces, dictates that a minimum level of normal force is required for controlled swimming. Since this minimum force is hydrodynamic and derived from the speed of the body, the birds have a minimal speed limitation for controlled swimming. This minimal swimming speed results in a minimum turning radius setting a limit to maneuvering in a tight space.
The long and flexible neck of cormorants may be an adaptation to overcome
such a limitation. Undoubtedly, the neck has additional functions, such as in
head stabilization for vision, but the ability to move a neck that is as long
as the body independently of the body can help the bird catch an escaping
fish. The minimal turning radius found in the present study was, on average 32
cm. The length of the neck plus the head of a great cormorant reaches 40% of
the total length of the body or 
0.34 m for a 0.85 m-long bird [fig. 1 in
Ribak et al. (Ribak et al.,
2005)]. The close similarity between the length of the neck and
the minimum turning radius means that the length of the cormorant neck is just
enough to capture small prey that could otherwise outmaneuver the larger and
faster cormorant. Smaller more maneuverable prey can find refuge from a faster
and larger predator by escaping into the `inner circle of safety' defined by
the minimum radius of turning of the predator, which is proportional to the
body mass and therefore much larger than that of the smaller prey
(Howland, 1974;
Weihs and Webb, 1984). The
long neck of the cormorant can allow the predator to reach into this inner
circle and intercept the prey. Such capability would be a great advantage for
a predator that must keep a fast swimming speed underwater.
In theory, the long and flexible neck of cormorants could also have a
hydrodynamic function. It should be noted that a 34 cm-long cylinder with a
mean diameter of 3 cm, moving through the water at 1.35 m s–1
(Fig. 4), with its long axis
perpendicular to the flow, can generate a hydrodynamic force as high as 10 N.
This force is twice as high as the estimate for buoyancy of great cormorants
at 1 m depth used in the present study. This force would also be high compared
with the normal forces estimated for the body and tail
(Fig. 9). However, in our
experiment the birds were seen to make very little use of this option. Normal
forces produced by the neck only peaked at 1 N
(Fig. 9). The neck is flexible
so that it can follow the curved trajectory during a maneuver and generate
minimal drag. By allowing the neck to deviate slightly from this trajectory,
the neck can move at an AoA producing forces normal to its length. During the
experiment, the birds were seen to bend their neck considerably while
maneuvering. The measured AoA of the different neck sections was not
necessarily small but these angles changed along the neck so that positive AoA
in sections close to one end of the neck were negative for sections closer to
the other end of the neck. Hydrodynamic forces produced by the neck as a whole
were smaller than the potential according to the AoA of individual neck
sections because the forces from different sections of the neck tended to
cancel each other out. Thus, much of the hydrodynamic forces produced by the
neck were `wasted' as drag. This can be a consequence of the tight,
bell-shaped trajectory where the anterior section of the neck and head were
moving in front of the body, with the trajectory curving downwards while the
posterior section of the neck and the body were still following a path curving
upwards. For simple turns in one direction the neck function can be more
unidirectional and substantial. However, there is a more compelling
explanation as to why the neck is not used extensively for vertical maneuvers.
The tail generates a substantial portion of the hydrodynamic forces used for
turning and also controls the body orientation (pitch). If both the tail and
neck produce forces in the same direction, the moments produced by the tail
posterior to the body and by the neck anterior to the body will have opposite
signs and work against each other. Since the body needs to rotate during the
maneuver, the contribution of the neck to the forces available for turning
cannot be so high as to interfere with rotation of the body during the
maneuver.
Fig. 4 can be used to
represent the maneuvering capabilities of cormorants when maneuvering is
defined as the standardized minimal turning radius (in body lengths) for a
standardized swimming speed (body lengthss–1). An average
cormorant with a body length of 85 cm can turn at a radius of 0.38 body
length while swimming at a speed of 1.6 body lengthss–1. We
were unable to find comparable data for vertical maneuvers in other swimming
organisms. However, the vertical maneuverability of cormorants (as defined
above) matches the highest values of horizontal maneuverability (side turns)
recorded in cetaceans (i.e. at a swimming speed of 1.6 body lengths
s–1, cormorants can make tighter turns than most cetaceans)
[see fig. 7 in Fish (Fish,
2002)]. This result is probably a consequence of the long and
flexible neck of cormorants, which `inflates' body length compared to mass of
the body, thus reducing the standardized turning radius. The vertical
maneuverability of cormorants also matches values of horizontal
maneuverability recorded from two species of sea lions. However, the sea lions
were capable of making slower turns at a much smaller turning radius [0.1
body lengths, California sea lion: fig. 1 in Fish et al.
(Fish et al., 2003a); Steller
sea lion, fig. 6 in Cheneval et al.
(Cheneval et al., 2007)]. Sea
lions are highly flexible semi-aquatic predators actively seeking and chasing
fish at structurally complex locations
(Fish et al., 2003a). As such,
their maneuverability might be more similar to cormorants, which utilize the
aquatic environment solely for foraging whereas cetaceans are also designed
for stability during open water swimming at low energetic cost
(Fish, 2002;
Fish et al., 2003b).
In the transition to foraging in water, aquatic birds diverged into two
aquatic strategies. Some aquatic birds use their wings for swimming underwater
while others use their feet. The occurrence of both strategies shows that both
are successful. Evolution of wing-propelled divers focused on solving the
required dynamic scaling of wing propulsion to efficiently operate in both
water and air (Lovvorn et al.,
1999). By contrast foot-propelled birds separate propulsion
between water and air and can, therefore, remain specific for propulsion in
each medium. However, the present study reveals that the separation between
locomotion in water and air in foot-propelled cormorants requires a separate
maneuvering mechanism for each medium and therefore the development of a
specific pitch-control mechanism for motion underwater. Such a mechanism comes
at a price of elevated drag from the pitched body
(Ribak et al., 2005). This
suggests that cormorants are not designed for swimming underwater at minimal
energetic cost but rather are designed to match the dynamic lifestyle of
aquatic predators adapted for fast, maneuverable swimming in the realm of
positive buoyancy.
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